Genetic variation for expression of the sex determination pathway genes in Drosophila melanogaster

Sequence polymorphisms result in phenotypic variation through the pathways of interacting genes and their products. We focused on transcript-level variation in the splicing pathway for sex determination – a model network defining downstream morphological characters that are dimorphic between males and females. Expression of Sex lethal, transformer, transformer2, doublesex, intersex and hermaphrodite was assayed with quantitative RT-PCR in 0- to 1-day-old adult males and females of 36 Drosophila melanogaster inbred lines. Abundant genetic variation in the transcript levels was found for all genes. Sex-specific splices had high concentrations in the appropriate sex. In the other sex, low but detectable concentrations were also observed. Abundances of splices strongly co-varied between sexes among genotypes, with little genetic variation strictly limited to one sex. The level of sexually dimorphic Yolk protein1 expression – an immediate downstream target of the pathway – was modelled as the target phenotype of the upstream sex determination pathway. Substantial genetic variation in this phenotype in males was explained by leaky splicing of female-specific transcripts. If higher transcript levels of the appropriate isoform of sex determination genes are beneficial in a sex, then stronger leakiness of the inappropriate transcript might be deleterious, perhaps contributing to the fitness trade-offs previously observed between the sexes.